Coon Gage R, Williams Leketha C, Matthews Adrianna, Diaz Roberto, Kevorkian Richard T, LaRowe Douglas E, Steen Andrew D, Lapham Laura L, Lloyd Karen G
Department of Microbiology, The University of Tennessee, Knoxville, Knoxville, TN, United States.
Department of Earth Sciences, University of Southern California, Los Angeles, CA, United States.
Front Microbiol. 2024 Nov 12;15:1455857. doi: 10.3389/fmicb.2024.1455857. eCollection 2024.
Molecular hydrogen is produced by the fermentation of organic matter and consumed by organisms including hydrogenotrophic methanogens and sulfate reducers in anoxic marine sediment. The thermodynamic feasibility of these metabolisms depends strongly on organic matter reactivity and hydrogen concentrations; low organic matter reactivity and high hydrogen concentrations can inhibit fermentation so when organic matter is poor, fermenters might form syntrophies with methanogens and/or sulfate reducers who alleviate thermodynamic stress by keeping hydrogen concentrations low and tightly controlled. However, it is unclear how these metabolisms effect porewater hydrogen concentrations in natural marine sediments of different organic matter reactivities.
We measured aqueous concentrations of hydrogen, sulfate, methane, dissolved inorganic carbon, and sulfide with high-depth-resolution and 16S rRNA gene assays in sediment cores with low carbon reactivity in White Oak River (WOR) estuary, North Carolina, and those with high carbon reactivity in Cape Lookout Bight (CLB), North Carolina. We calculated the Gibbs energies of sulfate reduction and hydrogenotrophic methanogenesis.
Hydrogen concentrations were significantly higher in the sulfate reduction zone at CLB than WOR (mean: 0.716 vs. 0.437 nM H) with highly contrasting hydrogen profiles. At WOR, hydrogen was extremely low and invariant (range: 0.41-0.52 nM H) in the upper 15 cm. Deeper than 15 cm, hydrogen became more variable (range: 0.312-2.56 nM H) and increased until methane production began at ~30 cm. At CLB, hydrogen was highly variable in the upper 15 cm (range: 0.08-2.18 nM H). Ratios of inorganic carbon production to sulfate consumption show AOM drives sulfate reduction in WOR while degradation of organics drive sulfate reduction in CLB.
We conclude more reactive organic matter increases hydrogen concentrations and their variability in anoxic marine sediments. In our AOM-dominated site, WOR, sulfate reducers have tight control on hydrogen via consortia with fermenters which leads to the lower observed variance due to interspecies hydrogen transfer. After sulfate depletion, hydrogen accumulates and becomes variable, supporting methanogenesis. This suggests that CLB's more reactive organic matter allows fermentation to occur without tight metabolic coupling of fermenters to sulfate reducers, resulting in high and variable porewater hydrogen concentrations that prevent AOM from occurring through reverse hydrogenotrophic methanogenesis.
分子氢由有机物发酵产生，并被包括氢营养型产甲烷菌和硫酸盐还原菌在内的生物在缺氧海洋沉积物中消耗。这些代谢过程的热力学可行性在很大程度上取决于有机物的反应性和氢浓度；低有机物反应性和高氢浓度会抑制发酵，因此当有机物匮乏时，发酵菌可能会与产甲烷菌和/或硫酸盐还原菌形成共生关系，后者通过保持低且严格受控的氢浓度来缓解热力学压力。然而，尚不清楚这些代谢过程如何影响不同有机物反应性的天然海洋沉积物中的孔隙水氢浓度。
我们在北卡罗来纳州怀特奥克河（WOR）河口碳反应性低的沉积物岩芯以及北卡罗来纳州瞭望角湾（CLB）碳反应性高的沉积物岩芯中，通过高深度分辨率测量了氢、硫酸盐、甲烷、溶解无机碳和硫化物的水溶液浓度，并进行了16S rRNA基因分析。我们计算了硫酸盐还原和氢营养型产甲烷作用的吉布斯自由能。
CLB的硫酸盐还原区中的氢浓度显著高于WOR（平均值：0.716对0.437 nM H），氢浓度分布差异极大。在WOR，上部15厘米处的氢含量极低且不变（范围：0.41 - 0.52 nM H）。在15厘米以下，氢变得更具变化性（范围：0.312 - 2.56 nM H）并增加，直到约30厘米处开始产生甲烷。在CLB，上部15厘米处的氢变化很大（范围：0.08 - 2.18 nM H）。无机碳生成与硫酸盐消耗的比率表明，在WOR中，厌氧氧化甲烷驱动硫酸盐还原，而在CLB中，有机物降解驱动硫酸盐还原。
我们得出结论，反应性更强的有机物会增加缺氧海洋沉积物中氢的浓度及其变化性。在以厌氧氧化甲烷为主的站点WOR中，硫酸盐还原菌通过与发酵菌形成共生体对氢进行严格控制，这由于种间氢转移导致观测到的方差较低。硫酸盐耗尽后，氢积累并变得可变，支持产甲烷作用。这表明CLB中反应性更强的有机物使得发酵能够在发酵菌与硫酸盐还原菌没有紧密代谢耦合的情况下发生，导致孔隙水氢浓度高且可变，从而阻止了通过逆向氢营养型产甲烷作用发生厌氧氧化甲烷。
